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Sand Fly and Leishmania Spp. Survey in Vojvodina (Serbia): First Detection

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Sand Fly and Leishmania Spp. Survey in Vojvodina (Serbia): First Detection Vaselek et al. Parasites & Vectors (2017) 10:444 DOI 10.1186/s13071-017-2386-z RESEARCH Open Access Sand fly and Leishmania spp. survey in Vojvodina (Serbia): first detection of Leishmania infantum DNA in sand flies and the first record of Phlebotomus (Transphlebotomus) mascittii Grassi, 1908 Slavica Vaselek1*, Nazli Ayhan2, Gizem Oguz3, Ozge Erisoz Kasap3, Sara Savić4, Trentina Di Muccio5, Luigi Gradoni5, Yusuf Ozbel6, Bulent Alten3 and Dušan Petrić1 Abstract Background: Leishmaniasis in Serbia was an endemic disease, and is considered to be eradicated for more than 40 years. In the past decade sporadic cases of canine leishmaniasis started to emerge for the first time in Vojvodina Province (previously non-endemic region of Serbia). Reports of introduced, and later on autochthonous cases of leishmaniasis alerted the possibility of disease emergence. The aim of this study was to bridge more than a half a century wide gap in entomological surveillance of sand fly vectors in Vojvodina, as well as to verify the presence of the vector species that could support Leishmania spp. circulation. Results: During the period 2013–2015, a total of 136 sand flies were collected from 48 of 80 surveyed locations. Four sand fly species of the genus Phlebotomus were detected: P. papatasi, P. perfiliewi, P. mascittii and P. neglectus. Detection of P. mascittii represents the first record of this species for the sand fly fauna in Vojvodina and in Serbia. All female specimens (n = 80) were tested for Leishmania spp. DNA, and three blood-fed P. papatasi specimens were positive (4%). One positive DNA sample was successfully amplified by ITS1 nPCR. The RFLP analysis of the resulting 350 bp fragment showed a typical pattern of L. infantum, and the ITS1 partial sequence blasted in GenBank confirmed 100% identity with L. infantum and L. donovani complex sequences. This result represents the first record of both Leishmania spp. and L. infantum DNA from sand flies in Vojvodina, and in Serbia. Conclusions: Presence of autochthonous canine leishmaniasis cases, records of Phlebotomus (Larroussius) species proven vectors of L. infantum (P. perfiliewi and P. neglectus)anddetectionofL. infantum DNA from wild caught (non-competent) vectors, prove that L. infantum is present in Vojvodina and indicates a probable circulation in the region. Keywords: Sand fly, Phlebotomus,Leishmaniasis,Leishmania infantum,Serbia * Correspondence: [email protected] 1Faculty of Agriculture, Department of Phytomedicine and Plant Protection, Laboratory for Medical Entomology, University of Novi Sad, Novi Sad, Serbia Full list of author information is available at the end of the article © The Author(s). 2017 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Vaselek et al. Parasites & Vectors (2017) 10:444 Page 2 of 8 Background P. papatasi, P. perfiliewi and P. neglectus [7]. The number The leishmaniases are major vector-borne diseases caused of specimens caught was rather low, with several samples by protozoan parasites belonging to the genus Leishmania. collected from various villages or from various houses in The parasites are transmitted to humans and other verte- the same village. Low sand fly diversity and abundance, as brates by the bite of infected female sand flies (Psychodi- well as the absence of human cases, resulted in the neglect dae, Phlebotominae). Around one billion of people are at of sand fly studies in this area for more than 60 years. risk of infection while number of reported cases per year is In the past decade, since 2006, cases of canine leishman- estimated at 0.7–1.3 million for cutaneous leishmaniasis iasis have started to emerge for the first time in Vojvodina. (CL) and 200,000–400,000 for visceral leishmaniasis (VL), Clinical symptoms and positive serological findings were causing over than 20,000 deaths annually [1]. first diagnosed in dogs that were imported or had travelled In Europe, leishmaniasis is endemic in all southern abroad to some of the Mediterranean countries with en- countries, with ~700 (3950 if Turkey is included) autoch- demic leishmaniasis [8]. Subsequent findings (2010–2013) thonous human cases reported every year [1]. The spread involved dogs that had never travelled from their home in of Leishmania infantum, causative agent of zoonotic VL Vojvodina [9]. This information suggested that both para- and CL in humans and domestic dogs (reservoir host) site and vector species are present in the region and impli- represents a major threat to Europe. Increasing dog and cated the possibility of autochthonous transmission. human travel, as well as the ongoing migrant crisis, pose a The aim of this study was to bridge more than a half a significant risk of L. infantum introduction into central century wide gap in entomological surveillance of sand fly Europe. Climate and land cover changes could also sup- vectors in Vojvodina, a very important transition region of port northward dispersal of vectors, establishment of Europe, as well as to verify the presence of the vector spe- seasonal biting rates matching those of southern Europe, cies that could support Leishmania spp. circulation. hence permitting autochthonous transmission [2]. In Serbia, leishmaniasis started to emerge after the Methods Second World War. Due to the composition and abun- Sand fly sampling dance of sand fly species at that time, poor hygienic and Cross-sectional entomological surveys were conducted health conditions in the post-war period, the disease between 2013 and 2015 in selected sample sites of the rapidly assumed an epidemic character [3]. The first Vojvodina Province (North Serbia). A total of 80 villages autochthonous case of VL was reported in 1945 [4]. were surveyed: 17 in 2013, 24 in 2014 and 39 in 2015. From 1945 to 1955, leishmaniasis spread in epidemic Surveys were conducted from the middle of May until waves from the southern parts of the country northwards, the middle of September. Due to the restricted funding, reaching its northernmost limit in central Serbia. After the sites sampled positive at first collection were not re- last major epidemic (1953), the number of new cases sampled, whereas negative locations were sampled again. started to diminish and, in the following years, the disease Sampling locations were partly chosen according to the appeared only sporadically. The last case of VL was re- available data about sand fly presence obtained during ported in 1968 [5], thereafter the disease was considered previous investigations (1948–1951) and data regarding eradicated. reported and/or suspected cases of canine leishmaniasis Sand fly research in Serbia was initiated in 1947, soon (2006–2013). The remaining locations are situated in after first cases of autochthonous VL emerged, and was areas without any data of sand fly and/or leishmaniasis terminated in 1990. During this period, the presence of presence. seven species of the genus Phlebotomus was recorded: Multiple sampling techniques were used to increase Phlebotomus papatasi, P. perfiliewi, P. tobbi, P. neglectus, the number of specimens sampled, as low abundance P. simici, P. sergenti and P. balcanicus [6]. The most in- was expected according to historical data. Indoor and tensive sand fly investigations were conducted during outdoor populations of sand flies were collected using a the VL epidemics, mainly in the infested areas. Following miniature Centre for Disease Control (CDC) light traps the disease spread, sand fly research was mainly focused (John W. Hock Company, model 512, Gainesville, Flor- on the south-east, east and central Serbia, leaving all ida, U.S.A.), dry-ice baited traps without light (NS2 other areas of country unexplored or partially explored. type), dry-ice baited traps with light, sticky papers and One of these less investigated and leishmaniasis-free mouth aspirators. Suction traps were operating over- region of Serbia includes Vojvodina Province, located in night, set at 16:00 h and collected at 08:00 h the next the north of the country. day. Traps were placed ~1.5 m above the ground inside Vojvodina was surveyed only briefly between 1949 and (CDC) and outside (traps with dry ice) of the houses 1951. Research was conducted irregularly (through the and animal shelters. Sticky traps (20 × 30 cm papers years and seasons) and only in a small number of loca- coated with commercial castor oil) were placed in holes tions. Studies revealed the presence of only three species: surrounding walls of animal shelters and houses, and all Vaselek et al. Parasites & Vectors (2017) 10:444 Page 3 of 8 other suitable sand fly resting places, for a period of four Results days. Indoor collections were performed during the day- During 2013–2015, a total of 136 sand flies were collected light using mouth aspirators. from 48 of 80 locations (Fig. 1). Four sand fly species of the genus Phlebotomus were identified: P. papatasi, P. per- Morphological identification of sand flies filiewi, P. mascittii and P. neglectus (Table 1). The majority All specimens collected were immediately transferred to of specimens (n = 130) belonged to P. papatasi (75 fe- 96% ethanol. Specimens were dissected; head and terminal males, 54 males, 1 undetermined) (GenBank: KY848828), segments of the abdomen were removed, cleared in Marc three females were identified as P. perfiliewi (GenBank: Andre solution and mounted in Berlese medium. The KY848829), two females as P. mascittii and one female as head and the tip of the abdomen were used for morpho- P. neglectus (GenBank: KY848830).
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